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Virulence profiles of enterotoxigenic, shiga toxin and enteroaggregative Escherichia coli in South African pigs

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Abstract

Enterotoxigenic Escherichia coli (ETEC) and shiga toxin E. coli (STEC) are important causes of colibacillosis in piglets. Recently, enteroaggregative E. coli heat-stable enterotoxin 1 (EAST-1) has been implicated in pig diarrhoea. This study investigated the prevalence of enterotoxin [heat-labile toxins (LT), heat-stable toxin a (STa), heat-stable toxin b (STb)], shiga toxins (Stx1, Stx2, Stx2e), enteroaggregative heat-stable E. coli (EAST-1), associated fimbriae (F4, F5, F6, F41, F18ab, F18ac) and non-fimbrial adhesins [adhesin involved in diffuse adherence 1 (AIDA-1), attaching and effacing factor, porcine attaching- and effacing-associated factor] in South African pigs. A total of 263 E. coli strains were isolated from Landrace (n = 24), Large White (n = 126), Duroc (n = 28) and indigenous (n = 85) breeds of piglets aged between 9 and 136 days. PCR was used in the analysis. Virulent genes were detected in 40.3 % of the isolates, of which 18.6, 0.4 and 17.5 % were classified as ETEC, STEC and enteroaggregative E. coli (EAEC), respectively. Individual genes were found in the following proportions: STb (19.01 %), LT (0.4 %), STa (3.4 %), St2xe (1.1 %) and EAST-1 (20.2 %) toxins. None of the tested fimbriae were detected in ETEC and STEC isolates. About one third of the ETEC and STEC isolates was tested negative for both fimbrial and non-fimbrial adhesins. Twenty-five pathotypes from ETEC-, EAEC- and STEC-positive strains were identified. Pathotypes EAST-1 (30.2 %), STb (13.2 %) and STb/AIDA-1 (10.4 %) were most prevalent. The study provided insight on possible causes of colibacillosis in South African pigs.

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Abbreviations

AIDA-1:

Adhesin involved in diffuse adherence 1

CF:

Colonisation factors

EAE:

Attaching and effacing factor

EAEC:

Enteroaggregative Escherichia coli

EAST-1:

Enteroaggregative E. coli heat-stable enterotoxin

ETEC:

Enterotoxigenic E. coli

LT:

Heat-labile toxins

PAA:

Porcine attaching- and effacing-associated factor

PCR:

Polymerase chain reaction

STa:

Heat-stable toxin a

STb:

Heat-stable toxin b

STEC:

Shiga toxin E. coli

Stx1:

Shiga toxins variant 1

Stx2:

Shiga toxins variant 2

Stx2e:

Shiga toxins variant 2e

References

  • Adams, M.R. and Moss. M.O. 2000. Food Microbiology. Royal Society of Chemistry, Cambridge

    Google Scholar 

  • Ateba, C.N. and Bezuidenhout, C.C. 2008. Characterisation of Escherichia coli O157 strains from humans, cattle and pigs in the North-West Province, South Africa. International Journal of Food Microbiology, 128, 181–188

    Article  PubMed  CAS  Google Scholar 

  • Ateba, C.N. and Mbewe, M. 2011. Detection of Escherichia coli O157: H7 virulence genes in isolates from beef, pork, water, human and animal species in the northwest province, South Africa: public health implications. Research Microbiology, 162, 240–248

    Article  CAS  Google Scholar 

  • Blanco, M., Blanco, J.E., Gonzalez, E.A., Mora, A., Jansen, W., Gomes, T., Zerbini, L.F., Yano, T., De Castro, A. and Blanco, J. 1997. Genes coding for enterotoxins and verotoxins in porcine Escherichia coli strains belonging to different O:K:H serotypes: relationship with toxic phenotypes. Journal of Clinical Microbiology, 35, 2958

    PubMed  CAS  Google Scholar 

  • Cai, H.Y., Archambault, M., Gyles, C.L. and Prescott, J.F. 2003. Molecular genetic methods in the veterinary clinical bacteriology laboratory: current usage and future applications. Animal Health Research Reviews, 4, 73–94

    Article  PubMed  CAS  Google Scholar 

  • Celemin, C., Rubio, P., Echeverria, P., and Suárez, S. 1995. Gene toxin patterns of Escherichia coli isolated from diseased and healthy piglets. Veterinary Microbiology 45, 121–127

    Article  PubMed  CAS  Google Scholar 

  • Chen, X., Gao, S., Jiao, X. and Liu, X.F. 2004. Prevalence of serogroups and virulence factors of Escherichia coli strains isolated from pigs with postweaning diarrhoea in eastern China. Veterinary Microbiology, 103, 13–20

    Article  PubMed  CAS  Google Scholar 

  • Cheng, D., Sun, H., Xu, J. and Gao, S. 2006. PCR detection of virulence factor genes in Escherichia coli isolates from weaned piglets with oedema disease and/or diarrhoea in China. Veterinary Microbiology, 115, 320–328

    Article  PubMed  CAS  Google Scholar 

  • Choi, C., Kwon, D. and Chae, C. 2001. Prevalence of the enteroaggregative Escherichia coli heat-stable enterotoxin 1 gene and its relationship with fimbrial and enterotoxin genes in E. coli isolated from diarrhoeic piglets. Journal of Veterinary Diagnostics Investigation, 13, 26–29

    Article  CAS  Google Scholar 

  • Department of Agriculture, Forestry and Fisheries. 2011. Trends in the Agriculture sector. South Africa, Pretoria, Department of Agriculture, Forestry and Fisheries. Available: http://www.daff.gov.za/docs/statsinfo/Trends_2011.pdf

  • De la Fe Rodriguez, P.Y., Coddens, A., Del Fava, E., Cortiñas Abrahantes, J., Shkedy, Z., Maroto Martin, L.O., Cruz Muñoz, E., Duchateau, L., Cox, E. and Goddeeris, B.M. 2011. High prevalence of F4+ and F18+ Escherichia coli in Cuban piggeries as determined by serological survey. Tropical Animal Health and Production, 43, 937–946

    Article  PubMed  Google Scholar 

  • Do, T., Stephens, C., Townsend, K., Wu, X., Chapman, T., Chin, J., McCormick, B., Bara, M. and Trott, D. 2005. Rapid identification of virulence genes in enterotoxigenic Escherichia coli isolates associated with diarrhoea in Queensland piggeries. Australian Veterinary Journal, 83, 293–299

    Article  PubMed  CAS  Google Scholar 

  • Estrada-Garcia, T., Lopez-Saucedo, C., Thompson-Bonilla, R., Abonce, M., Lopez-Hernandez, D., Santos, J.I., Rosado, J.L., DuPont, H.L. and Long, K. 2008. Diarrhoeagenic Escherichia coli Pathotypes association with Infection and Diarrhoea among Mexican Children: Atypical Enteropathogenic E. coli is Associated with Acute Diarrhoea. Journal of Clinical Microbiology, 47, 93–98

    Article  PubMed  Google Scholar 

  • Fairbrother, J.M., Nadeau, É., Gyles, C.L. 2005. Escherichia coli in postweaning diarrhoea in pigs: an update on bacterial types, pathogenesis, and prevention strategies. Animal Health Research Reviews, 6, 17–40

    Article  PubMed  CAS  Google Scholar 

  • Henton, M. 2010. Zoonotic diseases of pigs [Online]. Available: http://www.sapork.biz/zoonotic-diseases-of-pigs-2/ [Accessed 29 July 2011 at 11:59 am

  • Lee, S.I., Kang, S.G., Kang, M.L. and Yoo, H.S. 2008. Development of multiplex polymerase chain reaction assays for detecting enterotoxigenic Escherichia coli and their application to field isolates from piglets with diarrhoea. Journal of Veterinary Diagnostic Investigation, 20, 492–496

    Article  PubMed  Google Scholar 

  • Lee, S.I., Rayamahji, N., Lee, W.J., Cha, S.B., Shin, M.K., Roh, Y.M. and Sang, H.Y. 2009. Genotypes, antibiogram, and pulsed-field gel electrophoresis profiles of Escherichia coli strains from piglets in Korea. Journal of Veterinary Diagnostic Investigation, 21, 510–516

    Article  PubMed  Google Scholar 

  • Li, Y., Qiu, X., Li, H. and Zhang, Q. 2007. Adhesive patterns of Escherichia coli F4 in piglets of three breeds. Journal of Genetics and Genomics, 34, 591–599

    Article  PubMed  CAS  Google Scholar 

  • Matise, I., Cornick, N.A., Samuel, J.E. and Moon, H.W. 2003. Binding of Shiga toxin 2xe to porcine erythrocytes in vivo and in vitro. Infectious Immunology, 71, 5194–5201

    Article  CAS  Google Scholar 

  • Nagy, B., Arp, L., Moon, H. and Casey, T. 1992. Colonization of the small intestine of weaned pigs by enterotoxigenic Escherichia coli that lack known colonization factors. Veterinary Pathology 29, 239–246

    Article  PubMed  CAS  Google Scholar 

  • Ngeleka, M., Pritchard, J., Appleyard, G., Middleton, D.M. and Fairbrother, J.M. 2003. Isolation and association of Escherichia coli AIDA-I/STb, rather than EAST1 pathotype, with diarrhoea in piglets and antibiotic sensitivity of isolates. Journal of Veterinary Diagnostic Investigations, 15, 242–253

    Article  Google Scholar 

  • Oanh, T.K.N., Nguyen, V.K., De Greve, H., Goddeeris, B.M. 2012. Protection of piglets against oedema disease by maternal immunization with Stx2e toxoid. Infectious Immunology, 80, 469–473

    Article  CAS  Google Scholar 

  • Owusu-Asiedu, A., Nyachoti, C. and Marquardt, R. 2003. Response of early-weaned pigs to an enterotoxigenic Escherichia coli (K88) challenge when fed diets containing spray-dried porcine plasma or pea protein isolate plus egg yolk antibody, zinc oxide, fumaric acid, or antibiotic. Journal of Animal Sciences, 81, 1790–1798

    CAS  Google Scholar 

  • Rampoldi, A., Jacobsen, M.J., Bertschinger, H.U., Joller, D., Bürgi, E., Vögeli, P., Andersson L., Archibald, A.L., Fredholm, M. and Jørgensen, C.B. 2010. The receptor locus for Escherichia coli F4ab/F4ac in the pig maps distal to the MUC4–LMLN region, Mammalian Genome 22, 122–129

    Article  PubMed  Google Scholar 

  • Sargeant, H.R., McDowall, K.J., Miller, H.M. and Shaw, M.A. 2010. Dietary zinc oxide affects the expression of genes associated with inflammation: Transcriptome analysis in piglets challenged with ETEC K88. Veterinary Immunology and Immunopathology, 137, 120–129

    Article  PubMed  CAS  Google Scholar 

  • SAS. 2011. SAS User's Guide, Statistics. (Version 9.2). SAS Institute, Cary, NC, USA.

    Google Scholar 

  • South African Pork Producers. 2010., available online: http://www.sapork.com/

  • Veilleux, S. and Dubreuil, D.J. 2006. Presence of Escherichia coli carrying the EAST1 toxin gene in farm animals. Veterinary Research, 37, 3–13

    Article  PubMed  CAS  Google Scholar 

  • Vidotto, M.C., de Lima, N.C.S., Fritzen, J.T.T., de Freitas, J.C., Venancio, M.J. and Ono, M.A. 2009. Frequency of virulence genes in Escherichia coli strains isolated from piglets with diarrhoea in the North Parana State, Brazil. Brazilian Journal of Microbiology, 40, 199–204

    Article  Google Scholar 

  • Vu-Khac, H., Holoda, E., Pilipcinec, E., Blanco, M., Blanco, J., Mora, A., Dahbi, G., López, C. and González, E. 2006a. Serotypes, virulence genes, and PFGE profiles of Escherichia coli isolated from pigs with postweaning diarrhoea in Slovakia. BMC Veterinary Research, 2, 1–8

    Article  Google Scholar 

  • Wang, X.M., Jiang, H,X., Liao, X.P., Liu, J.H., Zhang, W.J., Zhang, H., Jiang, Z.G., Lü, D.H., Xiang, R. and Liu, Y.H. 2010. Antimicrobial resistance, virulence genes, and phylogenetic background in Escherichia coli isolates from diseased pigs. FEMS Microbiology Letters, 306, 15–21

  • Wang, X.M., Liao, X.P., Liu, S.G., Zhang, W.J., Jiang, H.X., Zhang, M.J., Zhu H.Q., Sun, Y., Sun, J., Li, A.X. and Lui, Y.H. 2011. Serotypes, Virulence Genes, and Antimicrobial Susceptibility of Escherichia coli Isolates from Pigs. Foodborne Pathogen and Diseases, 8, 687–692

    Article  CAS  Google Scholar 

  • Zajacova, Z.S., Konstantinova, L. and Alexa, P. 2011. Detection of virulence factors of Escherichia coli focused on prevalence of EAST1 toxin in stool of diarrhoeic and non-diarrhoeic piglets and presence of adhesion involving virulence factors in astA positive strains. Veterinary Microbiology, 154, 369–375

    Article  PubMed  Google Scholar 

  • Zhang, W., Zhao, M., Ruesch, L., Omot, A. and Francis, D. 2007. Prevalence of virulence genes in Escherichia coli strains recently isolated from young pigs with diarrhoea in the US. Veterinary Microbiology, 123, 145–152

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This study was funded by the University of KwaZulu-Natal Competitive Research Grant and the National Research Foundation. We thank Mary Ranketse for assisting with laboratory work. We are also grateful to the ARC, Animal Production Institute (Irene) and Middledrift farm for the pigs. The ARC-OVI Bacteriology Department provided E. coli reference samples.

Conflict of interest

The authors declare no potential conflicts of interest with respect to research, authorship and publication of this article.

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Authors and Affiliations

  1. Discipline of Genetics, School of Life Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville, 3209, Pietermaritzburg, South Africa

    Ramadimetja Prescilla Mohlatlole & Edgar Farai Dzomba

  2. Bacteriology Section, Agricultural Research Council–Onderstepoort Veterinary Institute, Private Bag X5, Onderstepoort, 0110, South Africa

    Evelyn Madoroba

  3. Biotechnology Platform, Agricultural Research Council, Private Bag X5, Onderstepoort, 0110, South Africa

    Farai Catherine Muchadeyi

  4. Discipline of Animal and Poultry Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville, 3209, Pietermaritzburg, South Africa

    Michael Chimonyo

  5. Agricultural Research Council, Animal Production Institute, Private Bag X2, 0062, Irene, South Africa

    Arnold Tapera Kanengoni

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  1. Ramadimetja Prescilla Mohlatlole
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  2. Evelyn Madoroba
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  3. Farai Catherine Muchadeyi
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  4. Michael Chimonyo
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  5. Arnold Tapera Kanengoni
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  6. Edgar Farai Dzomba
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Corresponding author

Correspondence to Edgar Farai Dzomba.

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Ethical standards

Animal handling and related experiments comply with animal ethics and experimental law of the Republic of South Africa.

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Mohlatlole, R.P., Madoroba, E., Muchadeyi, F.C. et al. Virulence profiles of enterotoxigenic, shiga toxin and enteroaggregative Escherichia coli in South African pigs. Trop Anim Health Prod 45, 1399–1405 (2013). https://doi.org/10.1007/s11250-013-0377-4

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